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Medium-term temporal stability of the helminth component community structure in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland

Published online by Cambridge University Press:  19 October 2004

A. BAJER ,
J. M. BEHNKE ,
A. PAWEŁCZYK ,
K. KULIŚ ,
M. J. SEREDA  and
E. SIŃSKI
A. BAJER
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
J. M. BEHNKE
Affiliation:
School of Biology, University of Nottingham, University Park, Nottingham NG7 2RD, UK
A. PAWEŁCZYK
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
K. KULIŚ
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
M. J. SEREDA
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland Current address: Department of Molecular Parasitology, Institute for Biology, Humboldt University Berlin, Philippstrasse. 13, 10115 Berlin, Germany.
E. SIŃSKI
Affiliation:
Department of Parasitology, Institute of Zoology, University of Warszawa, ul. Miecznikowa 1, 02-096 Warszawa, Poland
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Abstract

The structure of helminth communities in wild rodents is subject to seasonal variation, and is dependent on host age within years. Although between-year variation has been monitored, seldom has it been assessed rigorously by appropriate multifactorial analysis with potentially confounding factors taken into account. In this study we tested the null hypothesis that despite seasonal, host age and sex effects, helminth communities should show relative stability between years. Over a period of 3 years (1998–2000) we sampled bank vole (Clethrionomys glareolus) populations (total n=250) at 2 points in the year: in spring, at the start of the breeding season, and in autumn, after the cessation of breeding. In spite of seasonal differences and strong age effects, the between-year effects were surprisingly small. Measures of component community structure (Berger-Parker dominance index, the dominant species, S. petrusewiczi) did not vary, or varied only slightly from year to year. The majority of measures of infracommunity structure [Brillouin's index of diversity, prevalence of all helminths combined, prevalence and abundance of H. mixtum (the most prevalent helminth), mean species richness] did not differ significantly between years when other factors such as age, sex and seasonal variation had been taken into account. Some between-year variations were found (at the component community level, Simpson's index of diversity; at the infracommunity level, prevalence and abundance of S. petrusewiczi and abundance of all helminths combined), but even these were modest in comparison to seasonal and age differences, and were primarily attributable to S. petrusewiczi. We conclude that despite dynamic within-year fluctuations, helminth communities in bank voles in this region of Poland show relative stability across years. The sporadic occurrence of individual platyhelminths at low prevalence, makes little difference to the overall structure, which is largely maintained by the key roles played by the dominant intestinal nematodes of bank voles and the rarer species collectively.

Keywords

bank voleClethrionomys glareolushelminthsnematodescestodescomponent community
Type
Research Article
Information
Parasitology , Volume 130 , Issue 2 , February 2005 , pp. 213 - 228
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ABU-MADI, M. A., BEHNKE, J. M., LEWIS, J. W. & GILBERT, F. S. ( 2000). Seasonal and site specific variation in the component community structure of intestinal helminths in Apodemus sylvaticus from three contrasting habitats in south-east England. Journal of Helminthology 74, 7–15.Google Scholar
BAJER, A., PAWEŁCZYK, A., BEHNKE, J. M., GILBERT, F. S. & SIŃSKI, E. ( 2001). Factors affecting the haemoparasitic component community structure in bank voles (Clethrionomys glareolus) from the Mazury lake district region of Poland. Parasitology 122, 43–54.CrossRefGoogle Scholar
BEGON, M., HAZEL, S. M., BAXBY, D., BOWN, K., CAVANAGH, R., CHANTREY, J., JONES, T. & BENNETT, M. ( 1999). Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proceedings of the Royal Society of London, B 266, 1939–1945.CrossRefGoogle Scholar
BEGON, M., HAZEL, S. M., TELFER, S., BOWN, K., CARSLAKE, D., CAVANAGH, R., CHANTREY, J., JONES, T. & BENNETT, M. ( 2003). Rodents, cowpox virus and islands: densities, numbers and thresholds. Journal of Animal Ecology 72, 343–355.CrossRefGoogle Scholar
BEHNKE, J. M. ( 1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 1–70.CrossRefGoogle Scholar
BEHNKE, J. M., BARNARD, C. J., BAJER, A., BRAY, D., DINMORE, J., FRAKE, K., OSMOND, J., RACE, T. & SIŃSKI, E. ( 2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401–414.CrossRefGoogle Scholar
BEHNKE, J. M., LEWIS, J. W., MOHD ZAIN, S. N. & GILBERT, F. S. ( 1999). Helminth infections in Apodemus sylvaticus in southern England: interactive effects of host-age, sex and year on prevalence and abundance of infections. Journal of Helminthology 73, 31–44.Google Scholar
BEHNKE, J. M., LOWE, A., CLIFFORD, S. & WAKELIN, D. ( 2003). Cellular and serological responses in resistant and susceptible mice exposed to repeated infection with Heligmosomoides polygyrys bakeri. Parasite Immunology 25, 333–340.CrossRefGoogle Scholar
BUSH, A. O., LAFFERTY, K. D., LOTZ, J. M. & SHOSTAK, A. W. ( 1997). Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
CANNING, E. U., COX, F. E. G., CROLL, N. A. & LYONS, K. M. ( 1973). The natural history of Slapton Ley Nature Reserve: VI Studies on the parasites. Field Studies 3, 681–718.Google Scholar
CRAWLEY, M. T. ( 1993). GLIM for Ecologists. Blackwell Scientific Press, Oxford.
DASH, K. M., HALL, E. & BARGER, I. A. ( 1988). The role of arithmetic and geometric mean worm egg counts in faecal egg count reduction tests and in monitoring strategic drenching programs in sheep. Australian Veterinary Journal 65, 66–68.CrossRefGoogle Scholar
ELLIOTT, J. M. ( 1977). Some Methods for the Statistical Analysis of Samples of Benthic Invertebrates. Freshwater Biological Association, Cumbria, UK.
ELTON, C., FORD, E. B., BAKER, J. R. & GARDINER, A. D. ( 1931). The health and parasites of a wild mouse population. Proceedings of the Zoological Society of London 1931, 657–721.CrossRefGoogle Scholar
FERRARI, N., CATTADORI, I. M., NESPEREIRA, J., RIZZOLI, A. & HUDSON, P. J. ( 2004). The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecology Letters 7, 88–94.CrossRefGoogle Scholar
FURMAGA, S. ( 1957). Helminthofauna gryzoni polnych (Rodentia) okolic Lublina. Acta Parasitologica Polonica 5, 9–50.Google Scholar
GENOV, T. & YANCHEV, Y. ( 1981). Morphology and taxonomy of the nematodes of the genera Heligmosomoides Hall, 1916 and Heligmosomum Railliet et Henry, 1909 (Heligmosomidae Cram, 1927) from Bulgaria. Khelmintologiya 12, 8–30.Google Scholar
GREGORY, R. D. ( 1992). On the interpretation of host-parasite ecology: Heligmosomoides polygyrus (Nematoda) in wild wood mouse (Apodemus sylvaticus) populations. Journal of Zoology 226, 109–121.Google Scholar
GREGORY, R. D., MONTGOMERY, S. S. J. & MONTGOMERY, W. I. ( 1992). Population biology of Heligmosomoides polygyrus (Nematoda) in the wood mouse. Journal of Animal Ecology 61, 749–757.CrossRefGoogle Scholar
HANSSON, L. ( 1985). The food of bank voles, wood mice and yellow-necked mice. Symposia of the Zoological Society of London 55, 141–168.Google Scholar
HAUKISALMI, V. & HENTTONEN, H. ( 1990). The impact of climatic factors and host density on the long-term population dynamics of vole helminths. Oecologia 83, 309–315.CrossRefGoogle Scholar
HAUKISALMI, V. & HENTTONEN, H. ( 1993). Coexistence in helminths of the bank vole Clethrionomys glareolus. I. Patterns of co-occurrence. Journal of Animal Ecology 62, 221–229.Google Scholar
HAUKISALMI, V. & HENTTONEN, H. ( 2000). The variability of helminth assemblages and populations in the bank vole Clethrionomys glareolus. Polish Journal of Ecology 48 (Suppl.), 219–231.Google Scholar
HAUKISALMI, V., HENTTONEN, H. & TENORA, F. ( 1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.CrossRefGoogle Scholar
HAUKISALMI, V. & TENORA, F. ( 1993). Catenotaenia henttoneni sp.n. (Cestoda: Catenotaeniidae), a parasite of voles Clethrionomys glareolus and C. rutilus (Rodentia). Folia Parasitologica 40, 29–33.Google Scholar
HAZEL, S. M., BENNETT, M., CHANTREY, J., BOWN, K., CAVANAGH, R., JONES, T. R., BAXBY, D. & BEGON, M. ( 2000). A longitudinal study of an endemic disease in its wildlife reservoir: cowpox and wild rodents. Epidemiology and Infection 124, 551–562.CrossRefGoogle Scholar
HUSSEY, K. L. ( 1957). Syphacia muris vs S. obvelata in laboratory rats and mice. Journal of Parasitology 43, 555–559.Google Scholar
JANOVY, J. Jr., CLOPTON, R. E., CLOPTON, D. A., SNYDER, S. D., EFTING, A. & KREBS, L. ( 1995). Species density distributions as null models for ecologically significant interactions of parasite species in an assemblage. Ecological Modelling 77, 189–196.CrossRefGoogle Scholar
KENNEDY, C. R. & HARTVIGSEN, R. A. ( 2000). Richness and diversity of intestinal metazoan communities in brown trout Salmo trutta compared to those of eels Anguilla anguilla in their European heartlands. Parasitology 121, 55–64.CrossRefGoogle Scholar
KISIELEWSKA, K. ( 1970 a). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). 1. Structure and seasonal dynamics of helminth groupings in a host population in the Białowieza National Park. Acta Parasitologica Polonica 18, 121–147.Google Scholar
KISIELEWSKA, K. ( 1970 b). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). III. Structure of the helminth groupings in C. glareolus populations of various forest biocoenoses in Poland. Acta Parasitologica Polonica 18, 163–176.Google Scholar
KISIELEWSKA, K. ( 1970 c). Ecological organization of intestinal helminth groupings in Clethrionomys glareolus (Schreb.) (Rodentia). IV. Spatial structure of a helminth grouping within the host population. Acta Parasitologica Polonica 18, 177–196.Google Scholar
KISIELEWSKA, K. ( 1971). Intestinal helminths as indicators of the age structure of Microtus arvalis Pallas, 1778 population. Bulletin de L'Academie Polonaise des Sciences. Serie des Sciences Biologiques Cl.II, 19, 275–282.Google Scholar
KISIELEWSKA, K., FRACZAK, K., KRASOWSKA, I. & ZUBCZEWSKA, Z. ( 1973). Structure of the intestinal helminthocoenosis in the population of Microtus arvalis Pallas, 1778, and the mechanisms of its variability. Acta Parasitiologica Polonica 21, 71–83.Google Scholar
KISIELEWSKA, K. & ZUBCZEWSKA, Z. ( 1973). Intestinal helminths as indexes of reproduction dynamics in the host population – common vole. Acta Theriologica 18, 237–246.CrossRefGoogle Scholar
KOZAKIEWICZ, M. ( 1976). The weight of eye lens as the proposed age indicator of the bank vole. Acta Theriologica 21, 314–316.CrossRefGoogle Scholar
LANGLEY, R. & FAIRLEY, J. S. ( 1982). Seasonal variations in infestations of parasites in a wood mouse Apodemus sylvaticus population in the west of Ireland. Journal of Zoology 198, 249–261.CrossRefGoogle Scholar
LEWIS, J. W. ( 1968). Studies on the helminth parasites of the long-tailed field mouse, Apodemus sylvaticus sylvaticus from Wales. Journal of Zoology 154, 287–312.CrossRefGoogle Scholar
MARGOLIS, L., ESCH, G. W., HOLMES, J. C., KURIS, A. M. & SCHAD, G. A. ( 1982). The use of ecological terms in parasitology (report of an ad hoc committee of The American Society of Parasitologists). Journal of Parasitology 68, 131–133.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. ( 1988). Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice Apodemus sylvaticus. Journal of Helminthology 62, 78–90.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. ( 1989). Spatial and temporal variation in the infracommunity structure of helminths of Apodemus sylvaticus (Rodentia: Muridae). Parasitology 98, 145–150.CrossRefGoogle Scholar
MONTGOMERY, S. S. J. & MONTGOMERY, W. I. ( 1990). Structure, stability and species interactions in helminth communities of wood mice Apodemus sylvaticus. International Journal for Parasitology 20, 225–242.CrossRefGoogle Scholar
MORRIS, P. ( 1972). A review of mammalian age determination methods. Mammal Review 2, 69–104.CrossRefGoogle Scholar
OGDEN, C. G. ( 1971). Observations in the systematics of nematodes belonging to the genus Syphacia Seurat, 1916. Bulletin of the British Museum (Natural History) Zoology 20, 254–280.Google Scholar
O'SULLIVAN, H. M., SMAL, C. M. & FAIRLEY, J. S. ( 1984). A study of parasitic infestations in populations of small rodents (Apodemus sylvaticus and Clethrionomys glareolus) on Ross Island, Killarney. Journal of Life Sciences of the Royal Dublin Society 5, 29–42.Google Scholar
POULIN, R. ( 1993). The disparity between observed and uniform distributions: a new look at parasite aggregation. International Journal for Parasitology 23, 937–944.CrossRefGoogle Scholar
ROHLF, F. J. & SOKAL, R. R. ( 1995). Statistical Tables. Freeman W.H. and Company, San Francisco.
SHARPE, G. I. ( 1964). The helminth parasites of some small mammal communities. I. The parasites and their hosts. Parasitology 54, 145–154.Google Scholar
SOŁTYS, A. ( 1957). Badania nad robakami pasozytniczymi drobnych gryzoni Parku Narodowego w Białowieży. Acta Parasitologica Polonica 5, 487–504.Google Scholar
TENORA, F. ( 1967). Ecological study on helminths of small rodents of the Rohacska Dolina valley. Acta Scientiarum Naturalium Academiae Scientiarum Bohemoslovacae Brno 1, 163–207.Google Scholar
TENORA, F. & MESZAROS, F. ( 1975). Nematodes of the genus Syphacia Seurat, 1916 (Nematoda) – parasites of rodents (Rodentia) in Czechoslovakia and Hungary. Acta Universitatis Agriculturae 23, 537–554.Google Scholar
TENORA, F. & STANEK, M. ( 1995). Changes of the helminthofauna in several Muridae and Arvicolidae at Lednice in Moravia. II. Ecology. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 43, 57–65.Google Scholar
TENORA, F., WIGER, R. & BARUS, V. ( 1979). Seasonal and annual variations in the prevalence of helminths in a cyclic population of Clethrionomys glareolus. Holarctic Ecology 2, 176–181.CrossRefGoogle Scholar
TENORA, F. & ZEJDA, J. ( 1974). The helminth synusy of Clethrionomys glareolus in a lowland forest and its changes. Acta Scientiarum Naturalium Academiae Scientiarum Bohemoslovacae, Brno 6, 1–48.Google Scholar
WARDLE, R. A. & McLEOD, J. A. ( 1952). The Zoology of Tapeworms. The Univeristy of Minnesota Press, Minneapolis.
WASHINGTON, H. G. ( 1984). Diversity, biotic and similarity indices. A review with special relevance to aquatic ecosystems. Water Research 18, 653–694.CrossRefGoogle Scholar
WIGER, R., BARUS, V. & TENORA, F. ( 1978). Scanning electron microscopic studies on four species of the genus Syphacia (Nematoda, Oxyuridae). Zoologica Scripta 7, 25–31.CrossRefGoogle Scholar
WILSON, K. & GRENFELL, B. T. ( 1997). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle Scholar
ŻARNOWSKI, E. ( 1955). Parasitic worms of forest micromammalians (Rodentia and Insectivora) of the environment of Puławy (district Lublin) I. Cestoda. Acta Parasitologica Polonica 3, 279–343.Google Scholar